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Responses of Vallisneria natans (Lour.) Hara to the combined effects of Mn and pH

Ecotoxicology volume 28, pages 1177–1189 (2019)Cite this article

Abstract

Aquatic plants play a vital role in maintaining the health and stability of ecosystems and in ecological restoration of contaminated water bodies. Herein, a 21-day-long laboratory-scale experiment was designed to explore the growth and physiological responses of Vallisneria natans (Lour.) Hara (V. natans) to the combined effects of manganese (Mn, 5, 20, and 80 mg L−1) and pH (pH 4.0, 5.5, and 7.0). Our results showed the combined toxicity intensity was closely related to Mn concentration and the toxicity exhibited by Mn gradually strengthened with the decrease of pH level. High concentration of Mn stress significantly reduced plants leaf area, final leaf number, photosynthetic pigment content, RGR (relative growth rate) and biomass accumulation, but significantly increased the contents of malondialdehyde (MDA) and hydrogen peroxide (H2O2). At the same time, V. natans plants can resist the adverse stress by activating the antioxidant defense system, including superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and polyphenol oxidase (PPO) activities. Besides, V. natans tended to adjust the biomass allocation strategy and transferred more energy to the subsurface and the ramets and stolons parts under the combined stress. This experiment also showed that the increasing pH within a certain range could largely improve the removal rate of Mn (at highest by 84.28%). This may indicate the V. natans plant species can act as a promising tool for the Mn phytoremediation in aquatic environments which needs to be further explored by longer cycle field studies.

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References

  • Allan JD, Castillo MM (2007) Stream ecology. Springer, Dordrecht

    Google Scholar 

  • Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60:43–73

    CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    CAS  Google Scholar 

  • Bergmeyer HU (1984) Methods of enzymatic analysis. Academic press, New York, NY

    Google Scholar 

  • Campbel PGC, Stokes PM (1985) Acidification and toxicity of metals to aquatic biota. Can J Fish Aquat Sci 42:2034–2049

    Google Scholar 

  • Chen G, Liu X, Brookes PC, Xu J (2015a) Opportunities for phytoremediation and bioindication of arsenic contaminated water using a submerged aquatic plant: Vallisneria natans (Lour.) Hara. Int J Phytoremediat 17:249–255

    CAS  Google Scholar 

  • Chen M, Zhang LL, Li J, He XJ, Cai JC (2015b) Bioaccumulation and tolerance characteristics of a submerged plant (Ceratophyllum demersum L.) exposed to toxic metal lead. Ecotoxicol Environ Saf 122:313–321

    CAS  Google Scholar 

  • Clark RB, Pier PA, Knudsen D, Maranville JW (1981) Effect of trace element deficiencies and excesses on mineral nutrients in sorghum1. J Plant Nutr 3:357–374

    CAS  Google Scholar 

  • Cmc DM, Rodrã Guez JM, Carpio EA, Garcã APA, Stengel C, Berg M (2017) Arsenic, manganese and aluminum contamination in groundwater resources of Western Amazonia (Peru). Sci Total Environ 607:1437–1450

    Google Scholar 

  • Das AP, Ghosh S, Mohanty S, Sukla LB (2015) Advances in manganese pollution and its bioremediation. In: Sukla L, Pradhan N, Panda S, Mishra B (eds) Environmental microbial biotechnology. Springer, Cham, pp 313–328

    Google Scholar 

  • Das AP, Sukla LB, Pradhan N, Nayak S (2011) Manganese biomining: a review. Bioresour Technol 102:7381–7387

    CAS  Google Scholar 

  • Ferroni L, Baldisserotto C, Fasulo MP, Pagnoni A, Pancaldi S (2004) Adaptive modifications of the photosynthetic apparatus in Euglena gracilis Klebs exposed to manganese excess. Protoplasma 224:166–167

    Google Scholar 

  • François L, Fortin C, Campbell PGC (2007) pH modulates transport rates of manganese and cadmium in the green alga Chlamydomonas reinhardtii through non-competitive interactions: Implications for an algal BLM. Aquat Toxicol 84:123–132

    Google Scholar 

  • Ghorbanli M, Sepehr MF, Shekarkar N (2015) Interaction of pH and Mn on physiological parameters of Brassica oleracea L. J Plant Nutr 38:1383–1397

    CAS  Google Scholar 

  • Gonzalez EM, De Ancos B, Cano MP (1999) Partial characterization of polyphenol oxidase activity in raspberry fruits. J Agric Food Chem 47:4068–4072

    CAS  Google Scholar 

  • Han Y, Chen G, Chen Y, Shen Z (2015) Cadmium toxicity and alleviating effects of exogenous salicylic acid in Iris hexagona. Bull Environ Contam Toxicol 95:796–802

    CAS  Google Scholar 

  • Hauck M, Mulack C, Paul A (2002) Manganese uptake in the epiphytic lichens Hypogymnia physodes and Lecanora conizaeoides. Environ Exp Bot 48:107–117

    CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    CAS  Google Scholar 

  • Ho Y (2005) Effect of pH on lead removal from water using tree fern as the sorbent. Bioresour Technol 96:1292–1296

    CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:357–359

  • Hu R, Sun K, Su X, Pan YX, Zhang YF, Wang XP (2012) Physiological responses and tolerance mechanisms to Pb in two xerophils: Salsola passerina Bunge and Chenopodium album L. J Hazard Mater 205–206:131–138

    Google Scholar 

  • Huang C, Webb MJ, Graham RD (1993) Effect of pH on Mn absorption by barley genotypes in a chelate-buffered nutrient solution. Plant Soil 155–156:437–440

    Google Scholar 

  • Huang Y, Yang S, Long G, Gu M (2016) Manganese toxicity in sugarcane plantlets grown on acidic soils of Southern China. Plos One 11:e148956

    Google Scholar 

  • Issa AA, Abdek-Basset R, Adam MS (1995) Abolition of heavy metal toxicity on Kirchneriella lunaris (Chlorophyta) by Calcium. Ann Bot 75:189–192

    CAS  Google Scholar 

  • Jampeetong A, Brix H (2009) Effects of NaCl salinity on growth, morphology, photosynthesis and proline accumulation of Salvinia natans. Aquat Bot 91:181–186

    CAS  Google Scholar 

  • Jayasri MA, Suthindhiran K (2017) Effect of zinc and lead on the physiological and biochemical properties of aquatic plant Lemna minor: its potential role in phytoremediation. Appl Water Sci 7:1247–1253

    CAS  Google Scholar 

  • Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493

    CAS  Google Scholar 

  • Kováčik J, Babula P, Hedbavny J, Švec P (2014) Manganese-induced oxidative stress in two ontogenetic stages of chamomile and amelioration by nitric oxide. Plant Sci 215–216:1–10

    Google Scholar 

  • Lei Y, Korpelainen H, Li C (2007) Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere 68:686–694

    CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvent. Biochem Soc Trans 11:1982–1983

    Google Scholar 

  • Lidon FC, Barreiro MG, Ramalho JC (2004) Manganese accumulation in rice: implications for photosynthetic functioning. J Plant Physiol 161:1235–1244

    CAS  Google Scholar 

  • Lizieri C, Aguiar R, Kuki KN (2011) Manganese accumulation and its effects on three tropical aquatic macrophytes: Azolla caroliniana, Salvinia mínima and Spirodela polyrhiza. Rodriguésia 62:909–917

    Google Scholar 

  • Lizieri C, Kuki KN, Aguiar R (2012) The morphophysiological responses of free-floating aquatic macrophytes to a supra-optimal supply of manganese. Water Air Soil Pollut 223:2807–2820

    CAS  Google Scholar 

  • Madadkhah E, Lotfi M, Nabipour A, Rahmanpour S, Banihashemi Z, Shoorooei M (2012) Enzymatic activities in roots of melon genotypes infected with Fusarium oxysporum, f. sp. melonis race 1. Sci Hortic 135:171–176

    CAS  Google Scholar 

  • Millaleo R, Reyesdíaz M, Ivanov AG (2010) Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J Soil Sci Plant Nut 10:476–494

    Google Scholar 

  • Mu D, Ru S, Li T, Zhao J (2016) Effect of copper stress on physiological metabolism in sterile seedlings of Hydrilla verticillata (l. f.) royle. Acta Hydrobiol Sin 40:419–424. in Chinese

    Google Scholar 

  • Nan N, Zhang B, Li H, Zhang J (2011) Water quality purification ability of main wetland plant community in Hongze Lake. Res Soil Water Conserv 18:124–228. in Chinese

    Google Scholar 

  • Neculita CM, Rosa E (2019) A review of the implications and challenges of manganese removal from mine drainage. Chemosphere 214:491–510

    CAS  Google Scholar 

  • Neves MI, Prajapati DH, Parmar S, Aghajanzadeh TA, Hawkesford MJ, De Kok LJ (2017) Manganese toxicity hardly affects sulfur metabolism in Brassica rapa. In: De Kok L, Hawkesford M, Haneklaus S, Schnug E (eds) Sulfur metabolism in higher plants –fundamental, environmental and agricultural aspects. Proceedings of the International Plant Sulfur Workshop, Springer, Cham, pp 155–162

    Google Scholar 

  • Pan G, Liu W, Zhang H, Liu P (2018) Morphophysiological responses and tolerance mechanisms of Xanthium strumarium to manganese stress. Ecotoxicol Environ Saf 165:654–661

    CAS  Google Scholar 

  • Pollard AJ, Stewart HL, Roberson CB (2016) Manganese hyperaccumulation in Phytolacca americana L. from the Southeastern United States. Northeast Nat 16:155–162

    Google Scholar 

  • Pourrut B, Shahid M, Douay F (2013) Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants. In: Gupta D, Corpas F, Palma J (eds) Heavy metal stress in plants Springer, Berlin, Heidelberg, pp 121–147

    Google Scholar 

  • Rahman A, Hossain MS, Mahmud J, ahar K, Hasanuzzaman M, Fujita M (2016) Manganese-induced salt stress tolerance in rice seedlings: regulation of ion homeostasis, antioxidant defense and glyoxalase systems. Physiol Mol Biol Plants 22:291–306

    CAS  Google Scholar 

  • Rai UN, Sinha S, Tripathi RD, Chandra P (1995) Wastewater treatability potential of some aquatic macrophytes: removal of heavy metals☆. Ecol Eng 5:5–12

    Google Scholar 

  • Rengel Z, Marschner P (2010) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 168:305–312

    Google Scholar 

  • Romero DM, Ríos De Molina MC, Juárez ÁB (2011) Oxidative stress induced by a commercial glyphosate formulation in a tolerant strain of Chlorella kessleri. Ecotox Environ Safe 74:741–747

    CAS  Google Scholar 

  • Sakharov IY, Ardila GB (1999) Variations of peroxidase activity in cocoa (Theobroma cacao L.) beans during their ripening, fermentation and drying. Food Chem 65:51–54

    CAS  Google Scholar 

  • Sang Z, Ma L, Chen F (2011) Growth and physiological characteristics of Magnolia wufengensis seedlings under drought stress. Acta Bot Boreal-Occident Sin 31:109–115. in Chinese

    CAS  Google Scholar 

  • Sankar MS, Vega MA, Defoe PP, Kibria MG, Ford S, Telfeyan K, Neal A, Mohajerin TJ, Hettiarachchi GM, Barua S (2014) Elevated arsenic and manganese in groundwaters of Murshidabad, West Bengal, India. Sci Total Environ 488–489:570–579

    Google Scholar 

  • Santamaria AB (2008) Manganese exposure, essentiality & toxicity. Indian J Med Res 128:484–500

    CAS  Google Scholar 

  • Santos EF, Kondo Santini JM, Paixã OAP, Jãºnior EF, Lavres J, Campos M, Reis AR (2017) Physiological highlights of manganese toxicity symptoms in soybean plants: Mn toxicity responses. Plant Physiol Biochem 113:6–19

    CAS  Google Scholar 

  • Saygideger SD, Dogan M (2010) Combined effects of lead and different pH levels on lemna minor L., a free-floating aquatic macrophyte. American-Eurasian J Toxicol Sci 2:141–145

  • Sedmak JJ, Grossberg SE (1977) A rapid, sensitive, and versatile assay for protein using Coomassie brilliant blue G250. Anal Biochem. 79:544–552

    CAS  Google Scholar 

  • Shahid M, Khalid S, Abbas G, Shahid N, Nadeem M, Sabir M, Aslam M, Duma C (2015) Heavy metal stress and crop productivity. In: Hakeem K (eds) Crop production and global environmental issues. Springer, Cham, pp 1–25

    Google Scholar 

  • Shahid M, Pourrut B, Dumat C, Nadeem M, Aslam M, Pinelli E (2014) Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. In: Whitacre D (eds) Reviews of environmental contamination and toxicology. Springer, Cham, pp 1–44

    Google Scholar 

  • Shi H (2016) Experimental guidance of plant stress physiology. Science Press, Peking, China

    Google Scholar 

  • Spanic V, Vuletic MV, Abicic I (2017) Early response of wheat antioxidant system with special reference to Fusarium head blight stress. Plant Physiol Biochem 115:34–43

    CAS  Google Scholar 

  • Srivastava S, Dubey RS (2012) Nitric oxide alleviates manganese toxicity by preventing oxidative stress in excised rice leaves. Acta Physiol Plant 34:819–825

    CAS  Google Scholar 

  • El-Jaoual T, Cox DA (1998) Manganese toxicity in plants. J Plant Nutr 21:353–386

    CAS  Google Scholar 

  • Vadstrup M, Madsen TV (2010) Growth limitation of submerged aquatic macrophytes by inorganic carbon. Freshw Biol 34:411–419

    Google Scholar 

  • Veselý T, Trakal L, Száková J, Drábek O, Tejnecký V, Balíková M, Tlustoš P (2012) Removal of Al, Fe and Mn by Pistia stratiotes L. and its stress response. Cent Eur J Biol 7:1037–1045

    Google Scholar 

  • Wei Z, Stephen H, Gadd GM (2012) Biotransformation of manganese oxides by fungi: solubilization and production of manganese oxalate biominerals. Environ Microbiol 14:1744–1753

    CAS  Google Scholar 

  • Xin B, Chen B, Duan N, Zhou C (2011) Extraction of manganese from electrolytic manganese residue by bioleaching. Bioresour Technol 102:1683–1687

    CAS  Google Scholar 

  • Yan X, Yu D, Wang H, Wang J (2006) Response of submerged plant (Vallisneria spinulosa) clones to lead stress in the heterogenous soil. Chemosphere 63:1459–1465

    CAS  Google Scholar 

  • Zhang YJ, Mian YI, Wang C (2012) Research on phytoremediation of cadmium contaminated water by three submerged macrophytes. J Shanghai Ocean Univ 21:784–793. in Chinese

    Google Scholar 

  • Zhong G, Wu Z, Yin J, Chai L (2018) Responses of Hydrilla verticillata (L.f.) Royle and Vallisneria natans (Lour.) Hara to glyphosate exposure. Chemosphere 193:385–393

    CAS  Google Scholar 

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Acknowledgements

This research was funded by the National Natural Science Foundation of China (Nos: 31270410, 30970303, and 30670206).

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  1. Water Pollution Ecology Laboratory, College of Life Sciences, Wuhan University, Wuhan, 430072, PR China

    Jun Yin, Pei Fan, Guidi Zhong & Zhonghua Wu

  2. Shanghai Water Engineering Design & Research Institute Co., Ltd, Shanghai, 200061, PR China

    Jun Yin

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These authors contributed equally: Jun Yin, Pei Fan

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Yin, J., Fan, P., Zhong, G. et al. Responses of Vallisneria natans (Lour.) Hara to the combined effects of Mn and pH. Ecotoxicology 28, 1177–1189 (2019). https://doi.org/10.1007/s10646-019-02126-x

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Keywords

  • Mn
  • pH
  • Growth
  • Physiological responses
  • Vallisneria natans